Donor-strand exchange drives assembly of the TasA scaffold in Bacillus subtilis biofilms.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
18 11 2022
18 11 2022
Historique:
received:
29
03
2022
accepted:
03
11
2022
pubmed:
19
11
2022
medline:
23
11
2022
entrez:
18
11
2022
Statut:
epublish
Résumé
Many bacteria in nature exist in multicellular communities termed biofilms, where cells are embedded in an extracellular matrix that provides rigidity to the biofilm and protects cells from chemical and mechanical stresses. In the Gram-positive model bacterium Bacillus subtilis, TasA is the major protein component of the biofilm matrix, where it has been reported to form functional amyloid fibres contributing to biofilm structure and stability. Here, we present electron cryomicroscopy structures of TasA fibres, which show that, rather than forming amyloid fibrils, TasA monomers assemble into fibres through donor-strand exchange, with each subunit donating a β-strand to complete the fold of the next subunit along the fibre. Combining electron cryotomography, atomic force microscopy, and mutational studies, we show how TasA fibres congregate in three dimensions to form abundant fibre bundles that are essential for B. subtilis biofilm formation. Our study explains the previously observed biochemical properties of TasA and shows how a bacterial extracellular globular protein can assemble from monomers into β-sheet-rich fibres, and how such fibres assemble into bundles in biofilms.
Identifiants
pubmed: 36400765
doi: 10.1038/s41467-022-34700-z
pii: 10.1038/s41467-022-34700-z
pmc: PMC9674648
doi:
Substances chimiques
Bacterial Proteins
0
Amyloid
0
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
7082Subventions
Organisme : Wellcome Trust
ID : 202231/Z/16/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UP_1201/31
Pays : United Kingdom
Informations de copyright
© 2022. The Author(s).
Références
Mol Cell. 2006 Jun 23;22(6):831-842
pubmed: 16793551
FASEB J. 2019 Nov;33(11):12146-12163
pubmed: 31370706
Mol Microbiol. 2020 Dec;114(6):920-933
pubmed: 32491277
Proc Natl Acad Sci U S A. 2018 Mar 27;115(13):3237-3242
pubmed: 29531041
Proc Natl Acad Sci U S A. 2021 Aug 3;118(31):
pubmed: 34321357
Proc Natl Acad Sci U S A. 2020 Mar 3;117(9):4724-4731
pubmed: 32071243
Nature. 2021 Aug;596(7873):583-589
pubmed: 34265844
J Comput Chem. 2008 Aug;29(11):1859-65
pubmed: 18351591
J Struct Biol. 2015 Feb;189(2):147-52
pubmed: 25528570
Mol Microbiol. 2008 Sep;69(6):1399-410
pubmed: 18647168
Mol Microbiol. 2008 Jun;68(5):1117-27
pubmed: 18430133
Proc Natl Acad Sci U S A. 2010 Feb 2;107(5):2230-4
pubmed: 20080671
J Biol Chem. 2013 Jun 14;288(24):17559-68
pubmed: 23632024
Trends Microbiol. 2001 Jan;9(1):34-9
pubmed: 11166241
Cell Host Microbe. 2015 Nov 11;18(5):549-59
pubmed: 26567508
Science. 2017 Feb 24;355(6327):831-833
pubmed: 28232575
Cell. 2021 Nov 11;184(23):5740-5758.e17
pubmed: 34735796
J Mol Graph. 1996 Feb;14(1):33-8, 27-8
pubmed: 8744570
Structure. 2010 Oct 13;18(10):1244-60
pubmed: 20947013
J Struct Biol. 2015 Nov;192(2):216-21
pubmed: 26278980
Science. 2012 Jul 13;337(6091):236-9
pubmed: 22798614
Nat Commun. 2020 Apr 20;11(1):1859
pubmed: 32313019
J Comput Chem. 2017 Oct 15;38(27):2354-2363
pubmed: 28776689
Mol Microbiol. 2011 Jun;80(5):1155-68
pubmed: 21477127
Mol Microbiol. 2012 Aug;85(3):418-30
pubmed: 22716461
Nat Microbiol. 2020 Jun;5(6):830-837
pubmed: 32284566
J Chem Theory Comput. 2016 Jan 12;12(1):405-13
pubmed: 26631602
Mol Microbiol. 2018 Dec;110(6):897-913
pubmed: 29802781
Elife. 2020 Aug 20;9:
pubmed: 32815518
J Struct Biol. 2017 Jun;198(3):163-176
pubmed: 28193500
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
mBio. 2012 Aug 14;3(4):e00184-12
pubmed: 22893383
Microorganisms. 2021 Mar 04;9(3):
pubmed: 33806534
J Bacteriol. 2012 Jun;194(11):2781-90
pubmed: 22328672
Nucleic Acids Res. 2003 Jul 1;31(13):3381-5
pubmed: 12824332
Science. 2002 Feb 1;295(5556):851-5
pubmed: 11823641
Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11621-6
pubmed: 11572999
Mol Microbiol. 2010 Aug;77(4):1009-20
pubmed: 20572935
Proc Natl Acad Sci U S A. 2022 Jun 28;119(26):e2207037119
pubmed: 35727984
J Bacteriol. 1999 Mar;181(5):1664-72
pubmed: 10049401
Emerg Infect Dis. 2002 Sep;8(9):881-90
pubmed: 12194761
Nat Biotechnol. 2019 Apr;37(4):420-423
pubmed: 30778233
Annu Rev Microbiol. 2000;54:49-79
pubmed: 11018124
J Biol Chem. 2014 Oct 3;289(40):27513-25
pubmed: 25138218
J Bacteriol. 2014 Apr;196(8):1505-13
pubmed: 24488317
J Chem Theory Comput. 2009 Sep 8;5(9):2531-43
pubmed: 26616630
Nat Rev Microbiol. 2010 Sep;8(9):623-33
pubmed: 20676145
Nat Rev Microbiol. 2016 Aug 11;14(9):563-75
pubmed: 27510863
J Struct Biol. 2005 Oct;152(1):36-51
pubmed: 16182563
Mol Microbiol. 2005 Feb;55(3):739-49
pubmed: 15661000
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
pubmed: 15572765
Proc Natl Acad Sci U S A. 2022 Jan 25;119(4):
pubmed: 35042817
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21
pubmed: 20124702
Mol Microbiol. 2006 Feb;59(4):1216-28
pubmed: 16430695
Nucleic Acids Res. 2019 Jul 2;47(W1):W636-W641
pubmed: 30976793
Microorganisms. 2020 Dec 09;8(12):
pubmed: 33316961
Nat Microbiol. 2018 Dec;3(12):1451-1460
pubmed: 30297741
Nat Methods. 2017 Apr;14(4):331-332
pubmed: 28250466
J Bacteriol. 2001 May;183(9):2888-96
pubmed: 11292810
Mol Microbiol. 2006 Feb;59(4):1229-38
pubmed: 16430696
J Chem Phys. 2007 Jan 7;126(1):014101
pubmed: 17212484
J Struct Biol. 1996 Jan-Feb;116(1):71-6
pubmed: 8742726
Protein Sci. 2018 Jan;27(1):14-25
pubmed: 28710774
J Chem Theory Comput. 2013 Jan 8;9(1):687-97
pubmed: 26589065
Nat Rev Microbiol. 2013 Mar;11(3):157-68
pubmed: 23353768
J Struct Biol. 2012 Dec;180(3):519-30
pubmed: 23000701